Eco-evolutionary dynamics on Cyprus: a multitaxon approach to population differentiation within an isolated island

Project summary

In a recent account of the prospects of island biology studies 50 years after the, probably most seminal, ecological theory, the MacArthur-Wilson equilibrium theory of island biogeography (ETIB), have identified some of the most crucial under-explored subjects, in urgent need of further research. Among these, the study of clade differentiation and speciation patterns within islands appears as an important component of questions, such as in attempts to disentangle the role of arrival history in community assembly, in understanding the role of in situ evolution in ecosystem functioning, in assessing the role of gene flow in speciation, and in understanding why some lineages are richer than others using both phylogeographic and population genomic/genetic data. Despite the proliferation of phylogeographic and phylogenetic studies in the past few decades, research on evolutionary dynamics within isolated islands has not kept pace with larger-scale inter-island studies. Moreover, multitaxa approaches, with parallel studies of evolutionary diversification of several distinct lineages or even distant taxa within islands, are even rarer.
At the same time, the study of biodiversity has been revolutionized in the past decade by the combination of modern methods for species distribution modeling and the rapid advances of molecular techniques for evolutionary analyses. As such models have been applied for more than two decades now, it has been possible to evaluate their limitations and biases, and most researchers agree that a detailed knowledge of population genetics and lineage diversification is necessary for a reasonable evaluation of distribution modeling results.

The project aims to increase our understanding of eco-evolutionary processes under work on the long-isolated, environmentally diverse, and diversity-rich island of Cyprus. The studies of inter-island eco-evolutionary processes have been identified as high priority fields of research within the broad field of island biogeography. In addition, such information is necessary for building robust and dependable predictive models for the future of local biodiversity under climate change. Given that Cyprus is expected to become severely affected by the on-going climate change as higher temperatures, lower precipitation volumes and consequently desertification are threatening the eastern Mediterranean region, the proposed project is of high importance for biodiversity conservation.

Methodology outline

The project will estimate population genetics metrics and phylogenetic trees based on the application of the ddRADseq protocol (NGS on Illumina platform) on 7 study cases of endemic and/or other taxa with interesting distribution patterns on Cyprus that are potentially informative in terms of eco-evolutionary dynamics on the island. This analysis will be combined with cladochronological information based on traditional Sanger sequencing of mitochondrial and nuclear DNA markers of the same taxa, as well as information on environmental features and

preferences. Therefore, in order to be able to reach solid conclusions, it is important to study taxa for which we have the necessary background information on taxonomy, ecology and distribution. The use of endemic taxa is crucial also for exploring patterns and processes that can prove useful in conservation.

Taking advantage of our research group expertise our project focuses on the following taxa:

Terrestrial isopods (Crustacea, Isopoda, Oniscidea):

Case 1: Armadillo spp. (A. officinalis / A. n.sp.)
Two species of the genus have been found in Cyprus (Schmalfuss 1996 and coordinator’s personal data). The former is a widely distributed species in the Mediterranean, and is considered a taxon characteristic of Mediterranean-type ecosystems, the ‘animal equivalent’ of the olive tree. Some first analyses that have been made in our lab have shown unexpected genetic structure among population within Cyprus that need to be studied further. The second species has not been described yet, but is certainly an endemic of Cyprus, restricted to a few habitats rich in limestone, so that it is expected to show interesting patterns of genetic divergence. It shows morphological similarities with A. tuberculatus from Greece and SW Turkey, and A. albus from Israel. Both species will be studied in comparison with related species of the genus that are distributed in nearby areas (Greece, Israel etc), as well as with populations of the former species from these regions, so that we can identify the timing of Cyprus populations’ divergence and/or speciation.

Case 2: Porcellionides spp. (P. pruinosus / P. cyprius / P. cilicius)
This is a very interesting species group including a cosmopolitan species or ‘superspecies’ (P. pruinosus), a local endemic (P. cyprius) that is morphologically very similar to the former and has probably speciated from it, and a species restricted to a few regions in the eastern Mediterranean (P. cilicius) . A comparative study of these species, including also populations from nearby regions, is expected to reveal important eco-evolutionary processes.

Case 3: Levantoniscus spp. (L. makrisi / L. bicostulatus / L. wahrmani)
This is a genus recently described by the project coordinator and colleagues and included two species endemic on Cyprus (the former two, also described by the above-mentioned team) and one known only from nearby Near Eastern regions (the latter). They include endogean organisms (living deep in the soil) with restricted distribution within the island, constrained by high humidity levels that are sparsely encountered in these dry areas, and are expected to provide very insightful results, pertaining both to evolutionary history and climate change effects.

Case 4: Schizidium spp. (S. fissum / S. n. sp.)
This genus has been differentiated widely around eastern Mediterranean and the Middle East. On Cyprus there is one widely distributed epigean species (S. fissum) that can be found in a wide range of habitats and is also present at the nearby coastal areas of southern Turkey and the Lebanon , and one (or two) not yet described species of endogean species (coordinator’s personal data) with restricted occurrence on very humid sites on Mt. Troodos (Cedar valley) and Mt. Pentadaktylos (Akanthou). An analysis of the genus’ differentiation within Cyprus, taking also into account specimens from neighboring areas, can reveal important processes relevant to ecological speciation etc. The endogean species are also sensitive to climate change as they are dependent on high soil humidity.

Scorpions (Arachnida, Scorpiones):

Case 5: Mesobuthus cyprius / Buthus kunti
Two endemic species of two distinct genera in the family Buthidae occur on Cyprus, a unique pattern since these two genera are not found together elsewhere. Both species are widely distributed on the island and possibly exploit different microhabitats, even though this has not been studied in detail yet. The study of their populations’ genetic structure and their differentiation can also provide valuable eco-evolutionary insights.

Lizards (Chordata, Squamata):

Case 6: Acanthodactylus schreiberi
This lizard species, whose ecology and ecophysiology are already under study in the coordinator’s lab, occurs only on Cyprus and at a small nearby coastal area of southeastern Turkey. It is considered as Endangered in the IUCN Red List. There are contrasting views on its divergence from other congeneric groups (did the mainland population originate from the insular one or vice-

Case 7: Phoenicolacerta troodica
An endemic species of Cyprus, widely distributed in a variety of habitats. The study of various populations from different localities and habitat types can provide very useful evidence on local eco-evolutionary processes.

A workshop aiming to disseminate its results and highlight the emerged possibilities offered by the use on novel genomic tools in biodiversity research. Fore more info click here!

Dissemination activities

Scientific publications

Dimitriou, A.C., Antoniou, A., Alexiou, I., Poulakakis, N., Parmakelis, A. and Sfenthourakis, S., 2022. Diversification within an oceanic Mediterranean island: Insights from a terrestrial isopod. Molecular Phylogenetics and Evolution, 175, p.107585.

Dimitriou, A.C. and Sfenthourakis, S., 2022. An all-inclusive approach: A universal protocol for the successful amplification of four genetic loci of all Onscidea. MethodsX, 9, p.101762.

Campos-Filho, S.I., Dimitriou, A.C., Taiti, S., and Sfenthourakis, S., The genus Armadillo Latreille, 1802 (Oniscidea, Armadillidae) from Cyprus, with the descriptions of two new species, Zootaxa (Submitted)

Dimitriou, A.C., Campos-Filho, S.I., Georgiou, A., Taiti, S., and Sfenthourakis, S., Integrative taxonomy of Schizidium Verhoeff, 1901 (Oniscidea, Armadillidiidae) from Cyprus, with description of a new species (Under preparation).

Participation in scientific congresses

Dimitriou A.C., Alexiou, I., Parmakelis A., Sfenthourakis S. (2021). Patterns of genetic diversity of Armadillo officinalis (Isopoda:Oniscidea) within Cyprus. International Symposium on the Biology of Terrestrial Isopods, 11th ISTIB 12-14 July, Ghent, Belgium

Pagkalidou, E., Dimitriou, A. C., Sfenthourakis, S. (2021). Intra-island genetic diversification of the genus Porcellionides (Isopoda:Oniscidea) in Cyprus. International Symposium on the Biology of Terrestrial Isopods, 11th ISTIB 12-14 July, Ghent, Belgium

Campos-Filho, I.S., Dimitriou, A.C., Georgiou, A. and Sfenthourakis., S. (2022). The genus Schizidium Verhoeff, 1901 (Oniscidea, Armadillidiidae) in Cyprus XI Brazilian Crustacean Conference and The Crustacean Society Summer Meeting, XI CBC.TCS. June 6-9, Santos, Brazil

Workshop

Partners

Coordinator

Spyros Sfenthourakis

Spyros is an Associate Professor at UCY, head of the Ecology and Biodiversity Lab and currently Chair of the Department of Biological Sciences. His main research interests include island biogeography, community ecology, systematics and phylogeography, and is an expert in terrestrial isopod taxonomy having described more than 20 species new to science. He has coordinated and/or worked in several projects related to island biodiversity. He has more than 20 years experience in research, nature conservation, promoting and dissemination of science, participation in biodiversity related national fora (in Greece and Cyprus), and in conducting and coordinating research and conservation projects. He is also active in science communication, having given numerous public lectures and translated 20 public science books and textbooks.

Group members

Anna Papadopoulou - UCY

Anna is as an Assistant Professor at UCY and head of the recently founded Molecular Ecology and Evolution Lab. Her research focuses on the use of molecular genetic tools for the study of island biodiversity. She combines microevolutionary approaches (phylogeography and population genetics) with a macroecological perspective to understand the processes that generate and maintain biodiversity in island systems. She also applies DNA-based methodologies for large-scale biodiversity assessment and community ecology. Currently she is taking advantage of the enormous potential offered by Next-Generation Sequencing technologies and she uses genome-wide data to enhance all aspects of her research.

Nikos Poulakakis - UoC/NHMC

Nikos started at the University of Crete in 2009 as an Assistant Professor in the Department of Biology and PI of the Molecular Systematics Lab (MSL) of the Natural History Museum of Crete (NHMC), University of Crete. His interests focus on phylogenetics, systematics, phylogeography, and species delimitation of animals. A large component of his work combines information from genetics, genomics, ecology, paleogeography to understand the origin and evolutionary history of populations and to inform conservation management. A wide variety of new genomic tools, including RADseq for SNP-based phylogenetics, phylogeography and species delimitation are used by his research group. Finally, Additionally, much of his research focuses on techniques suitable for the extraction of ancient DNA from old museum specimens and fossil bones (i.e., giant Galapagos tortoises, and large mammals of the Mediterranean region, such as elephants, deer, hippos).

Alexandros Stamatakis - HITS

The Head of the computational molecular evolution group at HITS (Prof. Dr. A. Stamatakis) is an expert in bioinformatics, especially in applications related to phylogenetics, relevant software development, and NGS data processing, and has been managing an independent research group since early 2008. He is also one of the main organizers of the Summer School series on computational m molecular evolution (held every year since 2009). He was also head of the IT infrastructure group at HITS from 2010-2013 in conjunction with leading his research group and has received three awards for teaching excellence based on student evaluations from the dean of the department of computer science at KIT.

Andreas Dimitriou - UCY

Andreas is a PhD student at the Biodiversity and Ecology lab. His research focuses on the molecular phylogeny of terrestrial isopods (Isopoda: Oniscidea), a taxon with global distribution and long evolutionary history, represented by more than 3,700 species in some 500 genera and 37 families. He uses approaches pertinent to three different scales: at a large scale, he aims to clarify relationships among major clades of Oniscidea and other isopod suborders, at the intermediate scale, to reconstruct the phylogeny of all Oniscidea at the genus level, and at a local scale, to explore divergence patterns among species and populations within the long isolated island of Cyprus.

Theodora Antoniou - UCY

Theodora is a biologist who graduated from the University of Crete in 2017 and her thesis focused on the study of fossilised Pleistocene fish species and the palaeoenvironment of the area in which they were found. Following, in her MSc in Palaeobiology at the University of Bristol her research encompassed a morphometric analysis in order to identify the validity of an extinct Pleistocene hyena species found in Eurasia. Currently, her Ph.D, at the University of Cyprus, focuses on population genetics of four lizard species within Cyprus.

Funding

The Project EXCELLENCE/0918/0161 is co-financed by the European Regional Development Fund and the Republic of Cyprus through the Research and Innovation Foundation